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Microbial Methanogenesis in the Sulfate-Reducing Zone of Sediments in the Eckernförde Bay, SW Baltic Sea

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Microbial Methanogenesis in the Sulfate-Reducing Zone of Sediments in the Eckernförde Bay, SW Baltic Sea Biogeosciences, 15, 137–157, 2018 https://doi.org/10.5194/bg-15-137-2018 © Author(s) 2018. This work is distributed under the Creative Commons Attribution 3.0 License. Microbial methanogenesis in the sulfate-reducing zone of sediments in the Eckernförde Bay, SW Baltic Sea Johanna Maltby1,a, Lea Steinle2,1, Carolin R. Löscher3,1, Hermann W. Bange1, Martin A. Fischer4, Mark Schmidt1, and Tina Treude5,6 1GEOMAR Helmholtz Centre for Ocean Research Kiel, Department of Marine Biogeochemistry, 24148 Kiel, Germany 2Department of Environmental Sciences, University of Basel, 4056 Basel, Switzerland 3Nordic Center for Earth Evolution, University of Southern Denmark, 5230 Odense, Denmark 4Institute of Microbiology, Christian-Albrecht-University Kiel, 24118 Kiel, Germany 5Department of Earth, Planetary, and Space Sciences, University of California Los Angeles (UCLA), Los Angeles, California 90095-1567, USA 6Department of Atmospheric and Oceanic Sciences, University of California Los Angeles (UCLA), Los Angeles, California 90095-1567, USA apresent address: Natural Sciences Department, Saint Joseph’s College, Standish, Maine 04084, USA Correspondence: Johanna Maltby ([email protected]) and Tina Treude ([email protected]) Received: 4 February 2017 – Discussion started: 7 March 2017 Revised: 30 October 2017 – Accepted: 8 November 2017 – Published: 10 January 2018 Abstract. Benthic microbial methanogenesis is a known way of methanogenesis in the presence or absence of sul- source of methane in marine systems. In most sediments, fate reducers, which after the addition of a noncompetitive the majority of methanogenesis is located below the sulfate- substrate was studied in four experimental setups: (1) un- reducing zone, as sulfate reducers outcompete methanogens altered sediment batch incubations (net methanogenesis), for the major substrates hydrogen and acetate. The coex- (2) 14C-bicarbonate labeling experiments (hydrogenotrophic istence of methanogenesis and sulfate reduction has been methanogenesis), (3) manipulated experiments with the ad- shown before and is possible through the usage of non- dition of either molybdate (sulfate reducer inhibitor), 2- competitive substrates by methanogens such as methanol or bromoethanesulfonate (methanogen inhibitor), or methanol methylated amines. However, knowledge about the magni- (noncompetitive substrate, potential methanogenesis), and tude, seasonality, and environmental controls of this noncom- (4) the addition of 13C-labeled methanol (potential methy- petitive methane production is sparse. In the present study, lotrophic methanogenesis). After incubation with methanol, the presence of methanogenesis within the sulfate reduc- molecular analyses were conducted to identify key functional tion zone (SRZ methanogenesis) was investigated in sed- methanogenic groups during methylotrophic methanogene- iments (0–30 cm below seafloor, cm b.s.f.) of the season- sis. To also compare the magnitudes of SRZ methanogen- ally hypoxic Eckernförde Bay in the southwestern Baltic esis with methanogenesis below the sulfate reduction zone Sea. Water column parameters such as oxygen, temperature, (> 30 cm b.s.f.), hydrogenotrophic methanogenesis was de- and salinity together with porewater geochemistry and ben- termined by 14C-bicarbonate radiotracer incubation in sam- thic methanogenesis rates were determined in the sampling ples collected in September 2013. area “Boknis Eck” quarterly from March 2013 to Septem- SRZ methanogenesis changed seasonally in the up- ber 2014 to investigate the effect of seasonal environmental per 30 cm b.s.f. with rates increasing from March changes on the rate and distribution of SRZ methanogene- (0.2 nmol cm−3 d−1/ to November (1.3 nmol cm−3 d−1/ sis, to estimate its potential contribution to benthic methane 2013 and March (0.2 nmol cm−3 d−1/ to September emissions, and to identify the potential methanogenic groups (0.4 nmol cm−3 d−1/ 2014. Its magnitude and distribution responsible for SRZ methanogenesis. The metabolic path- appeared to be controlled by organic matter availability, Published by Copernicus Publications on behalf of the European Geosciences Union. 138 J. Maltby et al.: Microbial methanogenesis in the sulfate-reducing zone C = N, temperature, and oxygen in the water column, In marine sediments, methanogenesis activity is mostly revealing higher rates in the warm, stratified, hypoxic restricted to the sediment layers below sulfate reduction seasons (September–November) compared to the colder, due to the successful competition of sulfate reducers with oxygenated seasons (March–June) of each year. The ma- methanogens for the mutual substrates acetate and hydrogen jority of SRZ methanogenesis was likely driven by the (H2; Oremland and Polcin, 1982; Crill and Martens, 1986; usage of noncompetitive substrates (e.g., methanol and Jørgensen, 2006). Methanogens produce methane mainly methylated compounds) to avoid competition with sulfate from using acetate (acetoclastic methanogenesis) or H2 and reducers, as was indicated by the 1000–3000-fold increase carbon dioxide (CO2; hydrogenotrophic methanogenesis). in potential methanogenesis activity observed after methanol Competition with sulfate reducers can be relieved through addition. Accordingly, competitive hydrogenotrophic the usage of noncompetitive substrates (e.g., methanol or methanogenesis increased in the sediment only below methylated compounds, methylotrophic methanogenesis; Ci- the depth of sulfate penetration (> 30 cm b.s.f.). Members cerone and Oremland, 1988; Oremland and Polcin, 1982). of the family Methanosarcinaceae, which are known for The coexistence of sulfate reduction and methanogenesis has methylotrophic methanogenesis, were detected by PCR been detected in a few studies from organic-rich sediments, using Methanosarcinaceae-specific primers and are likely to e.g., salt-marsh sediments (Oremland et al., 1982; Buckley et be responsible for the observed SRZ methanogenesis. al., 2008), coastal sediments (Holmer and Kristensen, 1994; The present study indicates that SRZ methanogenesis is an Jørgensen and Parkes, 2010), or sediments in upwelling re- important component of the benthic methane budget and car- gions (Pimenov et al., 1993; Ferdelman et al., 1997; Maltby bon cycling in Eckernförde Bay. Although its contributions et al., 2016), indicating the importance of these environments to methane emissions from the sediment into the water col- for methanogenesis within the sulfate reduction zone (SRZ umn are probably minor, SRZ methanogenesis could directly methanogenesis). So far, however, environmental controls of feed into methane oxidation above the sulfate–methane tran- SRZ methanogenesis remain elusive. sition zone. The coastal inlet Eckernförde Bay (southwestern Baltic Sea) is an excellent model environment to study seasonal and environmental controls of benthic SRZ methanogene- sis. Here, the muddy sediments are characterized by high 1 Introduction organic loading and high sedimentation rates (Whiticar, 2002), which lead to anoxic conditions within the upper- After water vapor and carbon dioxide, methane is the most most 0.1–0.2 cm b.s.f. (Preisler et al., 2007). Seasonally hy- abundant greenhouse gas in the atmosphere (e.g., Hartmann poxic (dissolved oxygen < 63 µM) and anoxic (dissolved et al., 2013; Denman et al., 2007). Its atmospheric concen- oxygen D 0 µM) events in the bottom water of Eckernförde tration has increased more than 150 % since preindustrial Bay (Lennartz et al., 2014; Steinle et al., 2017) provide ideal times, mainly through increased human activities such as fos- conditions for anaerobic processes at the sediment surface. sil fuel usage and livestock breeding (Hartmann et al., 2013; Sulfate reduction is the dominant pathway of organic car- Wuebbles and Hayhoe, 2002; Denman et al., 2007). Deter- bon degradation in Eckernförde Bay sediments in the upper mining the natural and anthropogenic sources of methane 30 cm b.s.f., followed by methanogenesis in deeper sediment is one of the major goals for oceanic, terrestrial, and atmo- layers where sulfate is depleted ( 30 cm b.s.f.; Whiticar, spheric scientists to be able to predict further impacts on the 2002; Treude et al., 2005a; Martens et al., 1998; Fig. 1). This world’s climate. The ocean is considered to be a modest nat- methanogenesis below the sulfate–methane transition zone ural source for atmospheric methane (Wuebbles and Hayhoe, (SMTZ) can be intense and often leads to methane oversat- 2002; Reeburgh, 2007; EPA, 2010). However, research is still uration in the porewater below 50 cm of sediment depth, re- sparse on the origin of the observed oceanic methane, which sulting in gas bubble formation (Abegg and Anderson, 1997; automatically leads to uncertainties in current ocean flux es- Whiticar, 2002; Thießen et al., 2006). Thus, methane is trans- timations (Bange et al., 1994; Naqvi et al., 2010; Bakker et ported from the methanogenic zone (> 30 cm b.s.f.) to the sur- al., 2014). face sediment by both molecular diffusion and advection via Within the marine environment, the coastal areas (includ- rising gas bubbles (Wever et al., 1998; Treude et al., 2005a). ing estuaries and shelf regions) are considered the major Although upward-diffusing methane is mostly retained by source for atmospheric methane, contributing up to 75 % to the anaerobic oxidation of methane (AOM; Treude et al., the global ocean methane production (Bange et al., 1994). 2005a), a major part is reaching the sediment–water interface The majority of coastal methane is
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